Testosterone disrupts human collaboration by increasing egocentric choices

Abstract

Collaboration can provide benefits to the individual and the group across a variety of contexts. Even in simple perceptual tasks, the aggregation of individuals' personal information can enable enhanced group decision-making. However, in certain circumstances such collaboration can worsen performance, or even expose an individual to exploitation in economic tasks, and therefore a balance needs to be struck between a collaborative and a more egocentric disposition. Neurohumoral agents such as oxytocin are known to promote collaborative behaviours in economic tasks, but whether there are opponent agents, and whether these might even affect information aggregation without an economic component, is unknown. Here, we show that an androgen hormone, testosterone, acts as such an agent. Testosterone causally disrupted collaborative decision-making in a perceptual decision task, markedly reducing performance benefit individuals accrued from collaboration while leaving individual decision-making ability unaffected. This effect emerged because testosterone engendered more egocentric choices, manifest in an overweighting of one's own relative to others' judgements during joint decision-making. Our findings show that the biological control of social behaviour is dynamically regulated not only by modulators promoting, but also by those diminishing a propensity to collaborate.

Figures

Figure 1.

Experimental design. (a) Pairs of female participants (dyads) attended on two separate days in a blinded, randomized, placebo-controlled cross-over design. Both dyad members received identical treatment order. (b) Participants had blood taken before treatment and testing. (c) During testing dyad members sat in the same room viewing separate monitors. In a 2-alternative forced choice, design gratings were presented at two intervals, one containing a target grating with increased contrast. Each participant initially responded without consultation, providing measures of individual decision-making (Sindiv). If they disagreed, a joint decision was requested, which provided a measure of collaborative decision-making (Scollective). (d) Example psychometric function for dyad 1 under placebo. Proportion of trials reported as second interval is plotted against target contrast difference. Highly sensitive observers give steep functions with large slope (S). Here individuals (Sindiv) are red and green, and the dyad (Scollective) blue.

Figure 2.

Individuals derive a performance benefit from collaboration. The dyad's collaborative decisions were more sensitive (Scollective) than the individuals' decisions alone (Sindiv). Our metric for this performance benefit on the vertical axis is the difference between an individual's sensitivity and the cooperative sensitivity achieved by their dyad (Benefit of collaboration = Scollective− Sindiv). This benefit is attenuated by testosterone when collapsed across all 34 participants (Sindiv) and also when only the better (Smax) or worse (Smin) members of each dyad are included. All t-tests shown are paired. Error bars indicate s.e.m.

Figure 3.

Testosterone disrupts collaboration by increasing the egocentricity of decision-making. Each member of the dyad announced the dyad's joint decision in half the trials where such a collaborative decision was required. The sensitivity of collaborative decision-making hinges on the distribution in weighting attributed to one's own and the other's opinions. For each participant, we measured this weighting by the ratio of times they agreed with themselves (egocentric decisions) to agreement with the other's opinion (allocentric decisions). An egocentric–allocentric ratio of 1 means that participants weight their own and the other's original judgement equally. On placebo, there is trend towards egocentricity bias (one-sample, t33 = 1.8, p < 0.1)—an egocentricity bias that becomes marked on testosterone (one-sample, t33 = 3.0, p = 0.005). We show a paired t-test for testosterone versus placebo (t33 = 2.4, p < 0.05). Error bars indicate s.e.m.